Host-symbiont Interactions Research Articles

Contact and voter processes on the infinite percolation cluster as models of host-symbiont interactions

We introduce spatially explicit stochastic processes to model multispecies host-symbiont interactions. The host environment is static, modeled by the infinite percolation cluster of site percolation. Symbionts evolve on the infinite cluster through contact or voter type interactions, where each host may be infected by a colony of symbionts. In the presence of a single symbiont species, the condition for invasion as a function of the density of the habitat of hosts and the maximal size of the colonies is investigated in details. In the presence of multiple symbiont species, it is proved that the community of symbionts clusters in two dimensions whereas symbiont species may coexist in higher dimensions.

Disruption of the Termite Gut Microbiota and Its Prolonged Consequences for Fitness

The disruption of host-symbiont interactions through the use of antibiotics can help elucidate microbial functions that go beyond short-term nutritional value. Termite gut symbionts have been studied extensively, but little is known about their impact on the termite's reproductive output. Here we describe the effect that the antibiotic rifampin has not only on the gut microbial diversity but also on the longevity, fecundity, and weight of two termite species, Zootermopsis angusticollis and Reticulitermes flavipes. We report three key findings: (i) the antibiotic rifampin, when fed to primary reproductives during the incipient stages of colony foundation, causes a permanent reduction in the diversity of gut bacteria and a transitory effect on the density of the protozoan community; (ii) rifampin treatment reduces oviposition rates of queens, translating into delayed colony growth and ultimately reduced colony fitness; and (iii) the initial dosages of rifampin had severe long-term fitness effects on Z. angusticollis. Taken together, our findings demonstrate that the antibiotic-induced perturbation of the microbial community is associated with prolonged reductions in longevity and fecundity. A causal relationship between these changes in the gut microbial population structures and fitness is suggested by the acquisition of opportunistic pathogens and incompetence of the termites to restore a pretreatment, native microbiota. Our results indicate that antibiotic treatment significantly alters the termite's microbiota, reproduction, colony establishment, and ultimately colony growth and development. We discuss the implications for antimicrobials as a new application to the control of termite pest species.

Evolution of an endofungal lifestyle: Deductions from the Burkholderia rhizoxinica genome.

BackgroundBurkholderia rhizoxinica is an intracellular symbiont of the phytopathogenic zygomycete Rhizopus microsporus, the causative agent of rice seedling blight. The endosymbiont produces the antimitotic macrolide rhizoxin for its host. It is vertically transmitted within vegetative spores and is essential for spore formation of the fungus. To shed light on the evolution and genetic potential of this model organism, we analysed the whole genome of B. rhizoxinica HKI 0454 - a type strain of endofungal Burkholderia species.ResultsThe genome consists of a structurally conserved chromosome and two plasmids. Compared to free-living Burkholderia species, the genome is smaller in size and harbors less transcriptional regulator genes. Instead, we observed accumulation of transposons over the genome. Prediction of primary metabolic pathways and transporters suggests that endosymbionts consume host metabolites like citrate, but might deliver some amino acids and cofactors to the host. The rhizoxin biosynthesis gene cluster shows evolutionary traces of horizontal gene transfer. Furthermore, we analysed gene clusters coding for nonribosomal peptide synthetases (NRPS). Notably, B. rhizoxinica lacks common genes which are dedicated to quorum sensing systems, but is equipped with a large number of virulence-related factors and putative type III effectors.ConclusionsB. rhizoxinica is the first endofungal bacterium, whose genome has been sequenced. Here, we present models of evolution, metabolism and tools for host-symbiont interaction of the endofungal bacterium deduced from whole genome analyses. Genome size and structure suggest that B. rhizoxinica is in an early phase of adaptation to the intracellular lifestyle (genome in transition). By analysis of tranporters and metabolic pathways we predict how metabolites might be exchanged between the symbiont and its host. Gene clusters for biosynthesis of secondary metabolites represent novel targets for genomic mining of cryptic natural products. In silico analyses of virulence-associated genes, secreted proteins and effectors might inspire future studies on molecular mechanisms underlying bacterial-fungal interaction.

Spiroplasma as a model insect endosymbiont

Members of the genus Spiroplasma are actively motile and helical bacteria of the class Mollicutes, which are associated with a variety of arthropods and plants. Some spiroplasmas cause female-biased sex ratios of their host insects as a result of selective death of the male offspring during embryogenesis. Several strains of male-killing spiroplasmas have been successfully transfected into Drosophila melanogaster by haemolymph injection and maintained in laboratory fly stocks. Spiroplasma-Drosophila endosymbiosis represents an ideal model system for analysing the molecular mechanisms underlying host-symbiont interactions. The infection dynamics exhibited by the symbiont within the host, the effects of external and environmental factors on the symbiotic association and symbiont interactions with the host's immune system have been investigated using this system. Comparisons between a male-killing Spiroplasma strain and its non-male-killing variant revealed that, in addition to different male-killing abilities, they also differed in infection dynamics and resistance to host innate immunity. It is currently unclear whether these different phenotypes are interconnected to each other. However, if so, such pleiotropy could facilitate our understanding of the genetic and molecular mechanisms of the endosymbiotic system.

Quantitative comparison of bacterial communities in two Mediterranean sponges

Marine sponges can host in their tissues abundant and diverse bacterial communities. Lack of truly quantitative data on bacterial abundance and dynamics limits our understanding of the organization and functioning of these endobiotic communities. In this technical note, we describe a quantitative polymerase chain reaction approach to quantify the relative abundance of multiple clades of three major sponge-associated bacterial phyla: Chloroflexi, Acidobacteria, and Actinobacteria. To test our approach we used the Mediterranean sponges Spongia lamella and Aplysina aerophoba. We designed five out of the six primer sets used in our study. We tested the new primer sets for specificity and optimized their conditions. Our preliminary data showed that Spongia lamella had larger bacterial abundance than Aplysina aerophoba, except for one clade of Chloroflexi. The two Chloroflexi clades investigated in our study amplified a fraction of the Chloroflexi present in Spongia lamella and most of what is present in Aplysina aerophoba, suggesting a more diverse Chloroflexi population in Spongia lamella than in Aplysina aerophoba. This quantitative technique has a great potential to provide a rapid and robust assessment of sponge microbial target and could contribute to deciphering the complexity of these largely unknown host-symbiont interactions.

Virulence is context-dependent in a vertically transmitted aquatic host–microparasite system

Recent work has suggested that the outcomes of host–symbiont interactions can shift between positive, neutral and negative depending on both biotic and abiotic conditions. Even organisms traditionally defined as parasites can have positive effects on hosts under some conditions. For a given host–parasite system, the effects of infection on host fitness can depend on host vigour, route of transmission and environmental conditions. We monitored sublethal microsporidian infections in populations of Gammarus pseudolimnaeus (Amphipoda: Gammaridae) from four cool water streams in southwestern Michigan, USA. Our objectives were to: (i) infer the mechanism of transmission (horizontal, vertical or mixed) from observed effects of infection on host fitness, (ii) determine if the magnitude of the effects on host fitness is a function of parasite load (infection intensity) compared with simple presence or absence of infection, and (iii) determine if there is variation in parasite effects on host fitness in isolated populations. PCR and DNA sequence analyses revealed that there were two microsporidia present among the four host populations: Dictyocoela sp. and Microsporidium sp. PCR screening of a subset of infected hosts showed that Dictyocoela sp. accounted for 90% of infections and was present in all four G. pseudolimnaeus populations, while Microsporidium sp. was found in two populations but was only relatively common in one. We found very low prevalence in males (∼5%), but high prevalence in females (range: 37–85%). Female fitness was positively associated with infection in two streams, resulting from either higher fecundity or more reproductive bouts. Infection had a negative effect on the number of reproductive bouts in a third population, and no effect on fecundity in a fourth population. Infection intensity explained additional variation in fecundity in one population; females with intermediate infection intensity had higher fecundity than females with either light or heavy infection intensity. Given the high prevalence of infection in females compared with males and the generally weak negative fitness effects coupled with some positive fitness effects, it is likely that both Dictyocoela sp. and Microsporidium sp. are primarily vertically transmitted, feminizing microsporidia. Our results suggest that microsporidian effects on G. pseudolimnaeus fitness were context-dependent and varied with host sex and local environment.

Biomedical exploitation of the fungus-growing ant symbiosis

There is a constant need for discovering novel sources of compounds with antimicrobial properties, and recent studies support that symbiotic associations involving chemically mediated interactions may be a prominent source of novel compound discovery. Here I review a particularly promising natural system involving such interactions, the multipartite fungus-growing ant symbiosis. This includes a review of the ancient symbiosis involving intricate interactions between at least six symbionts, a review of the efforts that have been made in examining host-symbiont and symbiont-symbiont interactions, as well as the efforts made in identifying and characterizing chemical compounds mediating these interactions. Finally, I outline the prospects for future natural product discoveries from the system, touching on how advances in chemical analyses and whole-genome sequencing techniques will facilitate the process of natural product discovery of biomedical interest.

Huge Symbiotic Organs in Giant Scale Insects of the GenusDrosicha(Coccoidea: Monophlebidae) Harbor Flavobacterial and Enterobacterial Endosymbionts

Giant scale insects (Drosicha: Coccoldea: Monophlebidae) were investigated for their symbiotic organs and bacterial endosymbionts. Two types of bacterial 16S rRNA gene sequences, flavobacterial and enterobacterial, were consistently detected in D. corpulenta and D. pinicola. The former sequences formed a compact clade in the Bacteroidetes, allied to the symbionts of cushion and armored scales. The latter sequences formed a robust clade in the gamma-Proteobacteria, allied to enteric bacteria like Enterobacter aerogenes and Escherichia coli. Another type of 16S sequence derived from Wolbachia was also detected in D. pinicola. In-situ hybridization demonstrated that the flavobacterial and enterobacterial symbionts were localized in a pair of huge bacteriomes in the abdomen, the former in uninucleated peripheral bacteriocytes and the latter in syncytial central bacteriocytes. Electron microscopy confirmed the endocellular locations of the pleomorphic flavobacterial symbiont and the rod-shaped enterobacterial symbiont, and also revealed the location and fine structure of the Wolbachia symbiont in D. pinicola. Infection frequencies of the flavobacterial and enterobacterial symbionts were consistently 100% in populations of D. corpulenta and D. pinicola, while the Wolbachia symbiont exhibited 0% and 100% infection frequencies in D. corpulente and D. pinicola, respectively. Neither the flavobacterial symbiont nor the enterobacterial symbiont exhibited AT-biased nucleotide composition or accelerated molecular evolution. The huge bacteriomes of Drosicha giant scales would provide a useful system for investigating biochemical, physiological, and genomic aspects of the host-symbiont and symbiont-symbiont interactions.

Action of genotypical surrounding of host Drosophila melanogaster on biological effects of endosymbiont Wolbachia (strain wMelPop)

In this work, a comparative study of the structure of symbiotic bacteria Wolbachia (strain wMelPop decreasing the fly lifespan) in genotypically different Drosophila melanogaster, as well as the effect of the bacteria on the host cell ultrastructure was investigated out. As a result of special crossings, the Drosophila melanogaster [w]Trl362 and [w]Trlen82 lines, which are carried of mutations for the gene Trithorax-like, are synthesized (lines infected with Wolbachia are designated as [w]). The Drosophila melanogaster line free of Wolbachia was obtained by treatment with antibiotics of the initially infected [w]w1118 line. The complex of the used methods and approaches has allowed us to perform a comparative study of the morphology of cell structures for the first time before and after the infestation of insects with bacteria and to evaluate effect of the bacteria on viability and fertility of flies of these lines. Electron microscopy analysis has shown that the embryos of the analyzed lines contain typical Wolbachia in contact with various host cell compartments; the ultrastructural organization of the bacteria indicates the preservation of their functional activity. In the cytoplasm of embryos that are mutant for the gene Trithorax-like, morphologically atypical mitochondria were revealed, as well as Wolbachia (wMelPop) of unusual morphology with a modified form of membtane envelopes. The presence of Wolbachia in ovarian cells of the female mutant fly lines has been found to produce no effect on the amount of the female-ovipositioned eggs. It has been established for the first time that lifespans of the infected and Wolbachia-free Drosophila melanogaster mutant lines TM3 containing chromosome 3 as a balancer are equal. However, it is significantly shorter in the imago of the [w]w1118 line than in flies of the mutant lines. This has allowed us to suggest that either the chromosome-balancer TM3 or mutation of the gene Trl play an important role in the host-symbiont interactions. On checking this suggestion, it was found that the lifespan of homozygotes [w]Trl362 and [w]Trlen82 after the infection of flies with bacteria decreased markedly and was close to the lifespan of [w]w1118 line. The obtained data indicate that the chromosome-balancer TM3 can have a significant effect on the symbiont-host interaction.

The gut microbiota shapes intestinal immune responses during health and disease

Immunological dysregulation is the cause of many non-infectious human diseases such as autoimmunity, allergy and cancer. The gastrointestinal tract is the primary site of interaction between the host immune system and microorganisms, both symbiotic and pathogenic. In this Review we discuss findings indicating that developmental aspects of the adaptive immune system are influenced by bacterial colonization of the gut. We also highlight the molecular pathways that mediate host-symbiont interactions that regulate proper immune function. Finally, we present recent evidence to support that disturbances in the bacterial microbiota result in dysregulation of adaptive immune cells, and this may underlie disorders such as inflammatory bowel disease. This raises the possibility that the mammalian immune system, which seems to be designed to control microorganisms, is in fact controlled by microorganisms.

Genome size ofPachypsylla venusta(Hemiptera: Psyllidae) and the ploidy of its bacteriocyte, the symbiotic host cell that harbors intracellular mutualistic bacteria with the smallest cellular genome

Psyllids harbor the primary symbiont, Carsonella ruddii (gamma-Proteobacteria), within the cytoplasm of specialized cells called bacteriocytes. Carsonella has the smallest known cellular genome (160 kb), lacking numerous genes that appear to be essential for bacterial life. This raises the question regarding the genetic mechanisms of the host which supports the survival of Carsonella. Our preceding analyses have indicated that some of the genes that are encoded in the psyllid genome and which are highly expressed in the bacteriocyte are of bacterial origin. This implies that psyllids acquired genes from bacteria by lateral gene transfer (LGT) and are using these genes to maintain the primary symbiont, Carsonella. To reveal the complete picture of LGT from symbiotic bacteria to the genome of psyllids, whole genome analysis of psyllids is essential. In order to assess the feasibility of whole genome analysis of the host psyllid, the genome size of the hackberry petiole gall psyllid, Pachypsylla venusta, was estimated. Feulgen image analysis densitometry and flow cytometry demonstrated that the haploid genome size of P. venusta is 0.74 pg (724 Mb), verifying the feasibility of whole genome analysis. Feulgen image analysis densitometry further revealed that bacteriocytes of P. venusta are invariably 16-ploid. This higher ploidy may be essential to facilitate the symbiotic relationship with bacteria, as it appears to be a feature common to insect bacteriocytes. These results provide a foundation for genomics-based research into host-symbiont interactions.

Loline alkaloids for better protection of pastures from insect pests

Loline alkaloids are non-toxic to livestock and protect endophyte-infected fescue against insects. They are not present in perennial ryegrass (PRG) infected with its natural endophyte. PRG has been artificially infected with the loline-producing endophyte AR525, sourced from tall fescue. Keywords: endophyte, ryegrass, lolines, host-symbiont interaction

The Demosponge Amphimedon queenslandica: Reconstructing the Ancestral Metazoan Genome and Deciphering the Origin of Animal Multicellularity

INTRODUCTIONSponges are one of the earliest branching metazoans. In addition to undergoing complex development and differentiation, they can regenerate via stem cells and can discern self from nonself ("allorecognition"), making them a useful comparative model for a range of metazoan-specific processes. Molecular analyses of these processes have the potential to reveal ancient homologies shared among all living animals and critical genomic innovations that underpin metazoan multicellularity. Amphimedon queenslandica (Porifera, Demospongiae, Haplosclerida, Niphatidae) is the first poriferan representative to have its genome sequenced, assembled, and annotated. Amphimedon exemplifies many sessile and sedentary marine invertebrates (e.g., corals, ascidians, bryozoans): They disperse during a planktonic larval phase, settle in the vicinity of conspecifics, ward off potential competitors (including incompatible genotypes), and ensure that brooded eggs are fertilized by conspecific sperm. Using genomic and expressed sequence tag (EST) resources from Amphimedon, functional genomic approaches can be applied to a wide range of ecological and population genetic processes, including fertilization, dispersal, and colonization dynamics, host-symbiont interactions, and secondary metabolite production. Unlike most other sponges, Amphimedon produce hundreds of asynchronously developing embryos and larvae year-round in distinct, easily accessible brood chambers. Embryogenesis gives rise to larvae with at least a dozen cell types that are segregated into three layers and patterned along the body axis. In this article, we describe some of the methods currently available for studying A. queenslandica, focusing on the analysis of embryos, larvae, and post-larvae.

Cryptic diversity of the symbiotic cyanobacterium Synechococcus spongiarum among sponge hosts

Cyanobacteria are common members of sponge-associated bacterial communities and are particularly abundant symbionts of coral reef sponges. The unicellular cyanobacterium Synechococcus spongiarum is the most prevalent photosynthetic symbiont in marine sponges and inhabits taxonomically diverse hosts from tropical and temperate reefs worldwide. Despite the global distribution of S. spongiarum, molecular analyses report low levels of genetic divergence among 16S ribosomal RNA (rRNA) gene sequences from diverse sponge hosts, resulting either from the widespread dispersal ability of these symbionts or the low phylogenetic resolution of a conserved molecular marker. Partial 16S rRNA and entire 16S-23S rRNA internal transcribed spacer (ITS) genes were sequenced from cyanobacteria inhabiting 32 sponges (representing 18 species, six families and four orders) from six geographical regions. ITS phylogenies revealed 12 distinct clades of S. spongiarum that displayed 9% mean sequence divergence among clades and less than 1% sequence divergence within clades. Symbiont clades ranged in specificity from generalists to specialists, with most (10 of 12) clades detected in one or several closely related hosts. Although multiple symbiont clades inhabited some host sponges, symbiont communities appear to be structured by both geography and host phylogeny. In contrast, 16S rRNA sequences were highly conserved, exhibiting less than 1% sequence divergence among symbiont clades. ITS gene sequences displayed much higher variability than 16S rRNA sequences, highlighting the utility of ITS sequences in determining the genetic diversity and host specificity of S. spongiarum populations among reef sponges. The genetic diversity of S. spongiarum revealed by ITS sequences may be correlated with different physiological capabilities and environmental preferences that may generate variable host-symbiont interactions.

SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria

Root endosymbioses vitally contribute to plant nutrition and fitness worldwide. Nitrogen-fixing root nodulation, confined to four plant orders, encompasses two distinct types of associations, the interaction of legumes (Fabales) with rhizobia bacteria and actinorhizal symbioses, where the bacterial symbionts are actinomycetes of the genus Frankia. Although several genetic components of the host-symbiont interaction have been identified in legumes, the genetic basis of actinorhiza formation is unknown. Here, we show that the receptor-like kinase gene SymRK, which is required for nodulation in legumes, is also necessary for actinorhiza formation in the tree Casuarina glauca. This indicates that both types of nodulation symbiosis share genetic components. Like several other legume genes involved in the interaction with rhizobia, SymRK is also required for the interaction with arbuscular mycorrhiza (AM) fungi. We show that SymRK is involved in AM formation in C. glauca as well and can restore both nodulation and AM symbioses in a Lotus japonicus symrk mutant. Taken together, our results demonstrate that SymRK functions as a vital component of the genetic basis for both plant-fungal and plant-bacterial endosymbioses and is conserved between legumes and actinorhiza-forming Fagales.

Covalent attachment of proteins to peptidoglycan

Bacterial surface proteins are key players in host-symbiont or host-pathogen interactions. How these proteins are targeted and displayed at the cell surface are challenging issues of both fundamental and clinical relevance. While surface proteins of Gram-negative bacteria are assembled in the outer membrane, Gram-positive bacteria predominantly utilize their thick cell wall as a platform to anchor their surface proteins. This surface display involves both covalent and noncovalent interactions with either the peptidoglycan or secondary wall polymers such as teichoic acid or lipoteichoic acid. This review focuses on the role of enzymes that covalently link surface proteins to the peptidoglycan, the well-known sortases in Gram-positive bacteria, and the recently characterized l,d-transpeptidases in Gram-negative bacteria.

Identification ofAeromonas veroniiGenes Required for Colonization of the Medicinal Leech,Hirudo verbana

Most digestive tracts contain a complex consortium of beneficial microorganisms, making it challenging to tease apart the molecular interactions between symbiont and host. The digestive tract of Hirudo verbana, the medicinal leech, is an ideal model system because it harbors a simple microbial community in the crop, comprising the genetically amenable Aeromonas veronii and a Rikenella-like bacterium. Signature-tagged mutagenesis (STM) was used to identify genes required for digestive tract colonization. Of 3,850 transposon (Tn) mutants screened, 46 were identified as colonization mutants. Previously we determined that the complement system of the ingested blood remained active inside the crop and prevented serum-sensitive mutants from colonizing. The identification of 26 serum-sensitive mutants indicated a successful screen. The remaining 20 serum-resistant mutants are described in this study and revealed new insights into symbiont-host interactions. An in vivo competition assay compared the colonization levels of the mutants to that of a wild-type competitor. Attenuated colonization mutants were grouped into five classes: surface modification, regulatory, nutritional, host interaction, and unknown function. One STM mutant, JG736, with a Tn insertion in lpp, encoding Braun's lipoprotein, was characterized in detail. This mutant had a >25,000-fold colonization defect relative to colonization by the wild-type strain at 72 h and, in vitro, an increased sensitivity to sodium dodecyl sulfate, suggesting the presence of an additional antimicrobial property in the crop. The classes of genes identified in this study are consistent with findings from previous STM studies involving pathogenic bacteria, suggesting parallel molecular requirements for beneficial and pathogenic host colonization.

Host‐symbiont interactions of the primary endosymbiont of human head and body lice

The first mycetome was discovered more than 340 yr ago in the human louse. Despite the remarkable biology and medical and social importance of human lice, its primary endosymbiont has eluded identification and characterization. Here, we report the host-symbiont interaction of the mycetomic bacterium of the head louse Pediculus humanus capitis and the body louse P. h. humanus. The endosymbiont represents a new bacterial lineage in the gamma-Proteobacteria. Its closest sequenced relative is Arsenophonus nasoniae, from which it differs by more than 10%. A. nasoniae is a male-killing endosymbiont of jewel wasps. Using microdissection and multiphoton confocal microscopy, we show the remarkable interaction of this bacterium with its host. This endosymbiont is unique because it occupies sequentially four different mycetomes during the development of its host, undergoes three cycles of proliferation, changes in length from 2-4 microm to more than 100 microm, and has two extracellular migrations, during one of which the endosymbionts have to outrun its host's immune cells. The host and its symbiont have evolved one of the most complex interactions: two provisional or transitory mycetomes, a main mycetome and a paired filial mycetome. Despite the close relatedness of body and head lice, differences are present in the mycetomic provisioning and the immunological response.

Culture-independent characterization of the digestive-tract microbiota of the medicinal leech reveals a tripartite symbiosis.

Culture-based studies of the microbial community within the gut of the medicinal leech have typically been focused on various Aeromonas species, which were believed to be the sole symbiont of the leech digestive tract. In this study, analysis of 16S rRNA gene clone libraries confirmed the presence of Aeromonas veronii and revealed a second symbiont, clone PW3, a novel member of the Rikenellaceae, within the crop, a large compartment where ingested blood is stored prior to digestion. The diversity of the bacterial community in the leech intestinum was determined, and additional symbionts were detected, including members of the alpha-, gamma-, and delta-Proteobacteria, Fusobacteria, Firmicutes, and Bacteroidetes. The relative abundances of the clones suggested that A. veronii and the novel clone, PW3, also dominate the intestinum community, while other clones, representing transient organisms, were typically present in low numbers. The identities of these transients varied greatly between individual leeches. Neither time after feeding nor feeding on defibrinated blood caused a change in identity of the dominant members of the microbial communities. Terminal restriction fragment length polymorphism analysis was used to verify that the results from the clone libraries were representative of a larger data set. The presence of a two-member bacterial community in the crop provides a unique opportunity to investigate both symbiont-symbiont and symbiont-host interactions in a natural model of digestive-tract associations.

Horizontal endosymbiont transmission in hydrothermal vent tubeworms

Transmission of obligate bacterial symbionts between generations is vital for the survival of the host. Although the larvae of certain hydrothermal vent tubeworms (Vestimentifera, Siboglinidae) are symbiont-free and possess a transient digestive system, these structures are lost during development, resulting in adult animals that are nutritionally dependent on their bacterial symbionts. Thus, each generation of tubeworms must be newly colonized with its specific symbiont. Here we present a model for tubeworm symbiont acquisition and the development of the symbiont-housing organ, the trophosome. Our data indicate that the bacterial symbionts colonize the developing tube of the settled larvae and enter the host through the skin, a process that continues through the early juvenile stages during which the trophosome is established from mesodermal tissue. In later juvenile stages we observed massive apoptosis of host epidermis, muscles and undifferentiated mesodermal tissue, which was coincident with the cessation of the colonization process. Characterizing the symbiont transmission process in this finely tuned mutualistic symbiosis provides another model of symbiont acquisition and additional insights into underlying mechanisms common to both pathogenic infections and beneficial host-symbiont interactions.